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Hindawi Publishing CorporationJournal of Parasitology ResearchVolume 2012, Article ID 613132, 9 pagesdoi:10.1155/2012/613132
Research Article
Survey of the Synanthropic Flies Associated withHuman Habitations in Ubon Ratchathani Province ofNortheast Thailand
Tarinee Chaiwong,1 Thanyakarn Srivoramas,1 Kom Sukontason,2 Michelle R. Sanford,3
Kittikhun Moophayak,4 and Kabkaew L. Sukontason2
1 College of Medicine and Public Health, Ubon Ratchathani University, Warinchamrap, Ubon Ratchathani 34190, Thailand2 Faculty of Medicine, Chiang Mai University, Muang, Chiang Mai 50200, Thailand3 Pathology, Microbiology and Immunology, University of California, Davis, CA 95616, USA4 Bung Borapet Research and Training Center, Mahidol University Nakhonsawan Campus, Nakhonsawan 60000, Thailand
Correspondence should be addressed to Tarinee Chaiwong, tarinee [email protected]
Received 2 February 2012; Accepted 27 June 2012
Academic Editor: D. S. Lindsay
Copyright © 2012 Tarinee Chaiwong et al. This is an open access article distributed under the Creative Commons AttributionLicense, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properlycited.
Synanthropic fly surveys were performed to determine the species composition and abundance in Ubon Ratchathani provincein Northeast Thailand. Adult fly collections were conducted in various human habitations from two districts—Muang UbonRatchathani and Warinchamrap, at fresh-food markets, garbage piles, restaurants, school cafeterias, and rice paddy fields.Customized reconstructable funnel fly traps baited with 250 g of 1-day tainted beef were used for fly collections from September2010–February 2011. A total of 3,262 flies were captured, primarily consisting of three families including: Calliphoridae (6 species),Muscidae (3 species), and Sarcophagidae (11 species). The blow fly, Chrysomya megacephala, and the house fly, Musca domestica,were the dominant species collected from both districts at all collection sites. C. megacephala was predominant in paddy fields,restaurants and garbage piles, while M. domestica was numerically dominant in fresh-food markets and school cafeterias. Thecurrent survey identified various species of synanthropic flies with close associations to humans and with the ability to transmithuman pathogens in Ubon Ratchathani province; providing crucial information that may be used for developing control andsanitation management plans in this particular area.
1. Introduction
Synanthropic flies are those flies which are adapted to live inclose association with human habitations and are capable oftransmitting human pathogens either mechanically or bio-logically through this close relationship [1]. The link betweenhuman pathogens and fly transmission is due to the factthat adults feed on animal manure, trash, human excrement,and other decaying materials; readily moving between thesehabitats and food, food preparation surfaces, and humansthemselves [2]. Species of flies in the families Muscidae(house flies, latrine flies, and relatives), the Calliphoridae(blow flies and bottle flies), and the Sarcophagidae (fleshflies) have evolved to live in close association with human
development. There are over 50 species of synanthropic fliesthat have been reported to be associated with unsanitaryconditions and involved in the dissemination of humanenteropathogens in the environment [2]. In addition, thelarvae of these flies can also cause myiasis in human and live-stock [3]. The annoyance and public health risks associatedwith large populations of such flies is thus considerable.
Population densities of synanthropic flies are largely tiedto sanitation practices such that they are abundant in bothurban and rural areas where unsanitary conditions exist andare usually scarce when sanitary conditions are enforced[4]. Synanthropic fly population surveys are often conductedwith respect to enteropathogenic bacteria transmission [5–8]as well as some gastrointestinal parasites [9]. Another notable
2 Journal of Parasitology Research
feature of synanthropic fly populations is their propensityfor very rapid fluctuations in population density, often withadult numbers increasing by up to two orders of magnitudein a few days [10]. Thus, survey data that is collected overlong periods of time is required to capture the variationpresent in fly population densities, species composition, andrichness.
Synanthropic fly surveys have been conducted in manycountries of the Southeast Asian region. In Malaysia, thepredominant species recovered from surveys was M. domes-tica, but Sarcophaga spp. were not identified in these studies[11, 12]. In Thailand, surveys of Muscidae and Calliphoridaehave shown that M. domestica, and C. megacephala, are thetwo most prevalent species collected [13–16]. However, todate, no survey of the Sarcophagidae in Thailand has beenmade. Sarcophagidae are technically challenging to identifyand require examination of the male genitalia. Therefore,they are often not resolved to specific taxonomic resolution.
There is a great need for long-term surveys in Thailand ofthe three major synanthropic fly families to help determinethe effectiveness of sanitation practices, identify breedingsites, determine fly population fluctuations, determine theneed for control measures, and identify other insect speciesthat will inadvertently be affected by the chosen controlmethods [12]. The broad aim of this study was to determinethe synanthropic fly species composition in two areas ofUbon Ratchathani province in Northeast Thailand: MuangUbon Ratchathani and Warinchamrap districts, and toexamine population fluctuations, species composition, andabundance over a six-month study period. Baseline synan-thropic fly data will provide a means to generate integratedpest management plans for fly control and determine theimpact on the human community.
2. Materials and Methods
2.1. Collection. Fly surveys were conducted in two areasof Ubon Ratchathani province in Northeast Thailand—Muang Ubon Ratchathani district (the capital district ofthe province) and Warinchamrap district. Collections werecarried out at ten collection sites in each of the two districtsduring September 2010–February 2011. The collection sitesin each district were selected to include places wherepeople and flies would most likely interact with respectto enteropathogenic bacterial transmission, including fresh-food markets, garbage piles, restaurants, school cafeterias,and rice paddy fields where flies have the opportunity tofeed on both waste or unsanitary materials and human fooditems. The locality of each study area was georeferenced by aGarmin GPSMP 60CSx (Figure 1).
Adult fly collections were performed using individuallydeployed traps separated by approximately 1 km at each site.Customized funnel trap kits, designed by K. Sukontason[16], were deployed at each collection site in the morning(09:00–12:00). This trap consists of three components: (1)a polyvinyl chloride (PVC) frame box (30 × 30 × 30 cm),(2) a fly entrance module, and (3) a black fly net (30 × 30
× 30 cm) [16]. Each trap was baited with 250 g of 1-day-old beef tainted by leaving at room temperature for 24 hours[17]. The bait was kept in a translucent plastic container andplaced underneath the fly entrance module for the durationof trapping. After the three-hour collection period, the flynet was sealed, detached from the PVC frame, individuallyplaced in transparent plastic bags, and transported to thelaboratory at the College of Medicine and Public Health,Ubon Ratchathani University. At the laboratory, flies weresacrificed by placing the plastic bags from each trap into afreezer set at −20◦C for 15 min. All flies were counted, sexed,and identified the lowest taxonomic resolution possible usingthe taxonomic keys from Tumrasvin et al. [18] and Kurahashiand Chowanadisai [19].
2.2. Statistical Analysis. Following identification and abun-dance calculations for each site and species a chi-square testwas used to compare between the two predominant species,C. megacephala and M. domestica, from the five collectionsites. A Kruskal-Wallis Analysis of Variance (KW-ANOVA)followed by individual Mann-Whitney U tests were used totest for statistical differences among sites between the twopredominant species at each site in each district. To analyzethe abundance of C. megacephala and M. domestica overtime, the data were first transformed with the natural log(ln(X + 1)) to normalize the data. An analysis of variance(ANOVA) was then conducted for each species using theUnivariate General Linear Model (GLM) in SPSS 16.0 (SPSSGraduate Pack for Windows 16.0.1, Chicago, IL, USA). Themodel consisted of the variables location (Muang UbonRatchathani or Warinchamrap), month of collection and theinteraction between location and month. Significance for alltests was observed at the α = 0.05 level.
3. Results
During the six months sampled, a total of 3,262 flies werecollected from the ten collection sites. The surveys in MuangUbon Ratchathani and Warinchamrap districts yielded atotal of 2,257 and 1,005 flies, respectively (Tables 1 and2). Species from all three main synanthropic fly families ofMuscidae, Calliphoridae, and Sarcophagidae were recoveredfrom the surveys. The dominant species captured was theblow fly, C. megacephala, which ranked first in prevalence atall the collection sites, followed by M. domestica.
At the five collection sites in Muang Ubon Ratchathani,six species of blow flies were found with C. megacephala asthe most prevalent at 61.76% followed by Achoetandrus rufi-facies, Hemipyrellia ligurriens, Lucilia cuprina, Ceylonomyianigripes, and Hemipyrellia pulchra, subsequently. Withinthe Muscidae, M. domestica was most abundant at 13.20%and Boettcherisca peregrina was the dominant species ofSarcophagidae at 0.53% of the total flies collected (Table 1).The highest abundance of synanthropic flies were recoveredfrom the restaurant sites at 46.57% followed by schoolcafeterias, paddy fields, garbage piles, and fresh-food marketsat 23.79%, 16.54%, 7.74%, and 5.17% of total catch, respec-tively. The highest number of C. megacephala was recorded in
Journal of Parasitology Research 3
S
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Figure 1: Ten collection sites for adult fly collections in Muang Ubon Ratchathani and Warinchamrap districts, Ubon Ratchathani provinceNortheast Thailand.
4 Journal of Parasitology Research
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6 Journal of Parasitology Research
Muang Ubon Ratchathani from the restaurant sites, whereasthe lowest number was collected at the fresh-food marketsites (Table 1 and Figure 2(a)). M. domestica was also mostabundant at the restaurant site, but it was least abundantat the paddy field (Table 1 and Figure 2(a)). Collections ofC. nigripes and H. pulchra were made only at the paddyfield sites. Eleven species of flesh flies were recorded andscattered among all the collection sites (Table 1). The numberof females collected was greater than males at all collectionsites, with female to male ratio at 3.2 : 1, 4.6 : 1, 4.6 : 1, 5.2 : 1,and 7.6 : 1 in restaurant, school cafeterias, paddy fields, fresh-food markets, and garbage piles, respectively (Table 1).
In Warinchamrap, blow flies were numerically dominantwith C. megacephala being the primary species collected(51.44%). These observations differ with respect to therelative abundances of blow flies collected from the differentsites when compared to those recorded in Muang UbonRatchathani. H. ligurriens was the second most abundantspecies followed by A. rufifacies, L. cuprina, and H. pulchra,subsequently. No C. nigripes were collected from Warin-chamrap during this collection period. M. domestica rankedfirst among collected flies in Muscidae (22.19%); while B.peregrina was the dominant species of flesh fly at 0.50%of the total number collected (Table 2). The garbage pilesshowed the highest abundance of synanthropic flies col-lected from Warinchamrap (39.00%), followed by restaurant,paddy field, fresh-food market, and school cafeteria sites,respectively. The highest number of C. megacephala recordedin this district was at the garbage piles, whereas the lowestnumber was found at the fresh-food markets (Table 2 andFigure 2(b)). M. domestica was the most abundant at thefresh-food markets, but the lowest abundance was at thepaddy fields (Table 2 and Figure 2(b)). Six species of fleshflies were collected among all the sites. Similar to the resultsobserved in the Muang district, the number of femalescollected exceeded males, with the female:male ratio being3.5 : 1, 4.6 : 1, 5.2 : 1, and 7.9 : 1 in the paddy fields, restaurant,fresh-food markets, and school cafeterias, respectively. Incontrast to the Muang district, flies collected from garbagepiles indicated fewer females than males, with a female:maleratio of 0.65 : 1 (Table 2).
Fly abundance varied across collection site type. Acomparison of these two species among collection sitesshows that significantly more C. megacephala were collectedat the restaurant sites than any other type of site in theMuang Ubon Ratchathani (Figure 2(a)). The pattern for M.domestica is similar with significantly more flies collectedat restaurants than at any other site except for fresh-foodmarkets (Figure 2(a)). Fewer flies were collected at all sites inthe Warinchamrap district overall with significantly more C.megacephala collected in the restaurant and paddy fields sitesand significantly fewer M. domestica collected in the paddyfields (Figure 2(b)).
A significant difference was observed between the preva-lence of the two dominant species, C. megacephala andM. domestica, collected from Muang Ubon Ratchathaniand Warinchamrap at all collection sites (P < 0.001)(Table 3). Comparing the two districts over time illustratesthese differences, suggesting seasonality to C. megacephala
populations in the Muang Ubon Ratchathani, but not inWarinchamrap (Figure 3(a)). The ANOVA results showed astatistically significant difference between locations (F1,108 =11.493; P = 0.001) with significantly more C. megacephalacollected in Muang Ubon Ratchathani. There was not asignificant difference among months (F5,108 = 0.670; P =0.647) or in the interaction between location and month(F5,108 = 0.324; P = 0.898). This pattern was not clearlydefined in M. domestica (Figure 3(b)) and there was nosignificant difference in the mean abundance of house fliescollected between the two sites (F1,108 = 0.846; P = 0.360).There were also no significant differences found amongmonths (F5,108 = 0.754; P = 0.585) or in the interactionbetween location and month (F5,108 = 1.132; P = 0.348).
4. Discussion
The fly species collected in this survey represented 20 speciesin three families of Diptera (Muscidae, Calliphoridae, andSarcophagidae). C. megacephala was the dominant speciesin paddy field, restaurant, and garbage pile sites, which issimilar to the results of previous surveys of synanthropicflies in urban, suburban, forest, and mountain areas ofChiang Mai province in Northern Thailand [16]. On theother hand, previous surveys in Northern, Northeastern,and Central Thailand have suggested that M. domestica wasthe most abundant species in all the of the areas surveyedby Sucharit and Tumrasvin [15]. The numerical dominanceof M. domestica was also observed in previous studies inMalaysia [11, 12] and southern England [10]. It is interestingto note that M. domestica was not the dominant speciescollecting in this study, although the collection sites wereconsidered suitable breeding places for this species, whichhas strong associations with urban areas throughout theworld [4]. One reason for the differences between the currentstudy and others conducted in similar types of habitats, maybe the use of only 1-day tainted beef as bait in the presentstudy. Nurita et al. [11] suggested that adult blow flies aremore attracted to carrion and soggy, bloody or soiled hair,fur, or wool; using these resources as protein sources foregg maturation as well as for egg-laying substrate [20]. Thestrong association of house flies with fecal material and wetwaste may suggest that muscid flies may not be as stronglyattracted to a carrion based bait thus affecting collectionnumbers observed in this study. However, previous studiesin Thailand have indicated that 1-day tainted beef viscerawas the most suitable bait to use for collecting both blowfly and house fly in the field [16]. The species of flesh fliescollected in low numbers in this study may indicate a lack ofattraction to this particular type of bait or a lower populationabundance in these habitats.
This study revealed that more females were collected thanmales at almost all the study sites, with the exception ofgarbage piles in Warinchamrap district. This phenomenonwas similar to previous investigations in Thailand [14–16]and Malaysia for both Muscidae and Calliphoridae [12], inthe Czech Republic for Calliphoridae [21] and in Argentinafor Muscidae [21]. This sexual asymmetry may be attributed
Journal of Parasitology Research 7
900
800
700
600
500
400
300
200
100
0
Collections sites
Nu
mbe
r of
flie
s ca
ugh
t
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Restaurant Schoolcafeterias
Paddy fieldsGarbagepiles
C. megacephalaM. domestica
a d, e
b
e a, cd
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a, c
f
(a)
900
800
700
600
500
400
300
200
100
0
Collections sites
Nu
mbe
r of
flie
s ca
ugh
t
Fresh-foodmarkets
Restaurant Schoolcafeterias
Paddy fieldsGarbagepiles
C. megacephalaM. domestica
ad
b
d
a, b
a dd
b, c
e
(b)
Figure 2: The abundance of the two predominant species, C. megacephala and M. domestica collected from various human habitations inMuang Ubon Ratchathani (a) and Warinchamrap (b), Ubon Ratchathani province, Northeast Thailand during September 2010–February2011. Non-overlapping letters indicate a statistically significant difference in abundance among sites as determined by Kruskal-WallisANOVA and Mann-Whitney U comparisons for each species in each district at the α = 0.05 level.
Table 3: Comparison between the two predominant fly species, C. megacephala and M. domestica from five collection sites in UbonRatchathani province, Northeast Thailand during September 2010–February 2011.
SpeciesCollection sites
Chi-square (P-value)Fresh-food markets Restaurant Garbage piles School cafeterias Paddy fields
M. domestica 110 (67.0%) 37 (19.1%) 72 (23.0%) 36 (60.0%) 4 (2.5%)216.2 (<0.001)
C. megacephala 54 (33.0%) 157 (80.9%) 242 (77.0%) 24 (40.0%) 161 (97.5%)
75
60
45
30
15
0
Month
Sep Oct Nov Dec Jan Feb
LocationMuang Ubon RatchathaniWarinchamrap
Mea
n n
um
ber
ofC
. meg
acep
hala
cau
ght
(a)
75
60
45
30
15
0
Month
Sep Oct Nov Dec Jan Feb
LocationMuang Ubon RatchathaniWarinchamrap
Mea
n n
um
ber
ofM
. dom
esti
caca
ugh
t
(b)
Figure 3: Mean abundance (+/− SE) of C. megacephala (a) and M. domestica (b) over September 2010–February 2011 from each locationin Ubon Ratchathani province, Northeast Thailand.
8 Journal of Parasitology Research
to the fact that baits provide females with proteins neededfor ovary development and as potential oviposition sites.However, the present results differ from a previous studyin Thailand [15], reporting a 1 : 1 ratio of female:male ingarbage piles among species in Muscidae, Callipholidae, andSarcophagidae.
In the present study conducted in Muang UbonRatchathani and Warinchamrap, the dominant species wasC. megacephala except at the school cafeteria sites in theWarinchamrap district, where M. domestica was dominant.The significantly high abundance of C. megacephala atrestaurant sites in the Muang Ubon Ratchathani suggests anattractive resource at these sites. Bunchu et al. [17] foundmale and female C. megacephala were attracted to a widevariety of animal meat products as well as fresh fruits whichare likely to be found in restaurants during food preparation.Sucharit and Tumrasvin [15] reported that C. megacephalacollected from the Northeastern part of Thailand were foundat garbage piles more than in market places, which is similarto the trend observed in this study. It is possible that thegarbage piles are more attractive to C. megacephala becausethis location is composed of a variety of decomposingmaterials, such as vegetables and other decaying organicmatter. On the other hand, such types of decaying organicmatter are probably less abundant in fresh-food markets andschool cafeterias, potentially explaining the lower numberof C. megacephala captured at these sites. Such informationmay suggest that sanitation can have a significant impacton the availability of food and breeding places for synan-thropic flies, thus affecting fly population densities in thatparticular human habitation. Poor sanitation practices may,therefore, increase the potential interaction between flies,enteropathogenic bacteria, and people.
In conclusion, this study illustrates the diversity ofsynanthropic flies collected in various human localities inUbon Ratchathani province of Northeast Thailand. Fewlong-term fly survey datasets exist in Thailand and the datapresented here suggest seasonality in C. megacephala abun-dance (Figure 3(a)), however, differences among monthswere not significant for the survey dates analyzed in thisstudy. Additional long-term data should be collected todetermine if this trend is significant. Such information mayhelp in the development of control programs and in devel-oping education programs to emphasize the importance ofsanitation for fly management in this particular area. Thisis also the first survey of the Sarcophagidae associated withhuman developments in Thailand. These data may also proveuseful in the development of data on forensically relevantflies in this region of Thailand. Overall, these data begin theestablishment of a database that can be used to investigateother aspects of the synanthropic fly species associated withhuman environments and their ability to transmit pathogensto humans for this region of Thailand.
Acknowledgments
This study was financially supported by the ThailandResearch Fund, Office of the Higher Education Commission
and Ubon Ratchathani University (MRG5380283 to T.Chaiwong). The authors would like to thank the College ofMedicine and Public Health, Ubon Ratchathani Universityfor facilities.
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